Mechanisms of Ecological Divergence and Speciation: Genetic and Neurophysiological Bases for Fruit Volatile Discrimination Behavior in the Apple Maggot Fly (Rhagoletis pomonella)

Changes in behavior are often the impetus for speciation. Olfactory discrimination has played a key role in the ecologically differentiating apple and hawthorn infesting host races of the apple maggot fly, Rhagoletis pomonella (Walsh). Because Rhagoletis flies mate only on or near the fruit of their host plants, differences in fruit odor preference directly translate into mate choice and pre-zygotic reproductive isolation (RI), thus potentiating rapid divergence. However, little is known little about the neurological and genetic basis of host choice generating RI.

The objective of Chapter 2 of my dissertation was to determine how the neurosensory systems of apple and hawthorn flies differ to potentially affect fruit odor discrimination. Peripheral electrophysiology revealed that in both races there are two specific, colocalized olfactory sensory neurons (OSNs) sensitive to two critical behaviorally active volatiles emitted by ripe hawthorn (3-methyl-1-butanol) and apple (butyl hexanoate) fruit.

In Chapter 3, optical imaging, immunohistochemical, morphological, and electrophysiological techniques performed on apple and hawthorn flies implied that a reversal in the neurological processing of 3-methyl-1-butanol and butyl hexanoate occurs between the host races at the first synapse of the olfactory system, the antennal lobe.

In Chapter 4, I attempted to resolve the genetic architecture of host fruit odor discrimination based on a genome wide association (GWA) study. Apple and hawthorn flies phenotyped for their odor preference in a flight tunnel were then genotyped by restriction site associated DNA sequencing for 17, 567 single nucleotide polymorphisms (SNPs). No SNP displayed a significant association with behavior after correcting for multiple comparisons. I discuss whether host fruit odor discrimination is polygenic or due to large effect loci not detected in the GWA due to issues in phenotyping or marker coverage.

In conclusion, my research advanced the study of speciation in R. pomonella by revealing a potentially key aspect of the neurophysiology contributing to differential host choice. While questions remain concerning the genetics of host fruit odor discrimination in this system, studies synthesizing results from neurobiology, genetics, and ecology with evolutionary biology will continue to reinforce the central role that behavior plays in the origins of new species.